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Coevolution of Snake Venom Toxic Activities and Diet: Evidence That Ecological Generalism Favours Toxicological Diversity

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Coevolution of Snake Venom Toxic Activities and Diet: Evidence That Ecological Generalism Favours Toxicological Diversity toxins Article Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity Emma-Louise Davies and Kevin Arbuckle * Department of Biosciences, College of Science, Swansea University, Swansea SA2 8PP, UK; [email protected] * Correspondence: [email protected] Received: 4 September 2019; Accepted: 4 December 2019; Published: 6 December 2019 Abstract: Snake venom evolution is typically considered to be predominantly driven by diet-related selection pressures. Most evidence for this is based on lethality to prey and non-prey species and on the identification of prey specific toxins. Since the broad toxicological activities (e.g., neurotoxicity, coagulotoxicity, etc.) sit at the interface between molecular toxinology and lethality, these classes of activity may act as a key mediator in coevolutionary interactions between snakes and their prey. Indeed, some recent work has suggested that variation in these functional activities may be related to diet as well, but previous studies have been limited in geographic and/or taxonomic scope. In this paper, we take a phylogenetic comparative approach to investigate relationships between diet and toxicological activity classes on a global scale across caenophidian snakes, using the clinically oriented database at toxinology.com. We generally find little support for specific prey types selecting for particular toxicological effects except that reptile-feeders are more likely to be neurotoxic. We find some support for endothermic prey (with higher metabolic rates) influencing toxic activities, but differently from previous suggestions in the literature. More broadly, we find strong support for a general effect of increased diversity of prey on the diversity of toxicological effects of snake venom. Hence, we provide evidence that selection pressures on the toxicological activities of snake venom has largely been driven by prey diversity rather than specific types of prey. These results complement and extend previous work to suggest that specific matching of venom characteristics to prey may occur at the molecular level and translate into venom lethality, but the functional link between those two is not constrained to a particular toxicological route. Keywords: evolution; ecology; prey diversity; predator-prey coevolution; neurotoxicity; coagulotoxicity; cytotoxicity; nephrotoxicity Key Contribution: We provide the first broad-scale test of relationships between diet and the functional toxicological activities of snake venoms. Although we find limited support for interactions between particular prey types and particular types of toxicity, except in particular cases, we find that snakes consuming a greater diversity of prey types had a greater range of toxicological effects resulting for their venoms: ecological diversity begets toxicological diversity. 1. Introduction Venom has evolved many times throughout the animal kingdom, with most major lineages having evolved it at least once [1,2]. The frequent convergent evolution of venom systems is probably a consequence of two attributes. Firstly, all venoms are intricately tied to antagonistic coevolution [2] and this scenario is widely considered to favour the origin and elaboration of trait diversity [3–5]. Secondly, Toxins 2019, 11, 711; doi:10.3390/toxins11120711 www.mdpi.com/journal/toxins Toxins 2019, 11, 711 2 of 14 venom can fulfil multiple functions which are core to fitness, such as antipredator defence and prey capture, either because it is incidentally suited to functions other than those it has primarily been selected for [2], or because the venom system has specifically been selected for multiple functions [6,7]. The end result is that animal venoms are both taxonomically and functionally diverse in addition to the substantial chemical diversity widely recognized amongst toxinologists [1]. Amongst animal venoms, those of caenophidian (‘advanced’) snakes are the best studied, largely as a result of the global medical importance of venomous snakebite [8,9]. Despite the defensive nature of snakebites inflicted on humans, this is a secondary function in the sense that the main selective driver of snake venom evolution is prey subjugation [1,2,10]. Notwithstanding a range of other adaptive and non-adaptive processes that may have contributed to variation in snake venoms [11,12], a key role of diet-related selection is supported by a variety of types of evidence. The availability of different prey species will vary geographically, and their availability to an individual snake will vary with ontogeny, either via ontogenetic shifts in diet or simply in predation-relevant prey characteristics such as size. Consequently, several studies have looked for geographic or ontogenetic variation in venom composition or toxicity that may be explained by variation in prey. For instance, Daltry et al. [10] found that variation in the venom of the Malayan pitviper (Calloselasma rhodostoma) was related to both geographic and diet variation but that diet was the controlling factor, with geographic variation in venom as a result of geographic variation in diet. Similarly, a range of studies have found ontogenetic shifts in venom composition or toxicity which seem to correspond to diet shifts in the species in question [13–16], but it is typically difficult to exclude coincidental explanations in these cases. The possibility of coincidental ontogenetic shifts in both venom and diet is emphasised by studies which find a shift in one but not the other. For instance, despite sharing similar diet (differing mostly in size), juvenile and adult monocle cobras (Naja kaouthia) have notable differences in venom [17], while a shift from preying on lizards and frogs to preying on rodents as Gloyd’s cantil (Agkistrodon howardgloydi) grows is not associated with clear venom differences [18]. Some studies have related the toxicity of a venom (measured as median lethal dose, LD50) to different taxa that variably represent natural prey. Perhaps the best example of this work on snake venoms involves saw-scaled vipers of the genus Echis [19,20]. This relatively small genus contains dietary generalists, but with some species which predominantly feed on vertebrates and others which feed predominantly on arthropods [19,21]. The venom from species that prey more on arthropods is more toxic to scorpions [19], and in fact is more toxic to scorpions (of a species which they naturally prey upon) than to captive bred locusts [20], both suggesting that the venom of saw-scaled vipers has been selected for prey capture. Similar patterns have also been documented in brown tree snakes (Boiga irregularis), the venom of which is far more toxic to lizards and birds than to mammals [14], reflecting the focus of the diet on diapsids [22]. Furthermore, a shift to feeding on prey that does not require subjugation, such as eggs, appears to lead to reduced toxicity [11] and a general pattern of loss or degeneration of venom systems [23]. This again suggests a predominant role of diet in driving venom evolution since there is no obvious reason that, for instance, predation risk should typically change greatly following a shift of diet (as would be necessary for inferring a primarily defensive role). However, as striking and informative as these relationships are, coevolution can lead to defensive toxin resistance to snake venom in prey species [24,25], obscuring clear positive relationships between toxicity and natural diet. Moreover, given that the ultimate function of a predatory snake venom is to incapacitate rather than kill prey [26], which may not be mechanistically identical processes, the standard use of lethality as a measure of toxicity blurs the interpretation of such data from an evolutionary ecological perspective to some degree. In addition to the above studies on whole-venom toxicity, evidence for a relationship between snake venom and diet has been documented in the form of prey-specific toxins, especially from snakes not traditionally considered to have particularly potent venom (resulting from limited activity on mammals such as humans) [27]. For instance, the three-finger toxin (3FTx) ‘denmotoxin’ was isolated Toxins 2019, 11, 711 3 of 14 from Boiga dendrophila venom which was ~100 times more potent on bird than mammal neurotoxicity assays in vitro [28]. The diet of this species is fairly generalist, including many mammals, but is predominantly comprised of diapsids (birds and reptiles) [29–31] suggesting that future study of the activity of denmotoxin on reptiles would be interesting. Nevertheless, the frequent presence of mammals in the diet of B. dendrophila highlights the imperfect correlation between diet and prey-specific toxins, although other mammal-specific toxins may remain to be discovered from this species. Consistent with the latter suggestion, and another example of prey-specific toxins, two 3FTxs described from the venom of Spilotes sulphureus have contrasting prey-specificity, with one active against mammals but not lizards, and another active against lizards but not mammals [32]. Note that prey-specific toxins are not restricted to 3FTxs; different forms of snake venom metalloproteinases (SVMPs) isolated from Bothrops neuwiedi have been shown to vary greatly in their toxicity to mammals vs birds [33]. Such evidence demonstrates that individual toxins may be selected to target particular prey types and provides a good mechanistic basis for how diet-driven selection of venom could operate. However, the effects of particular
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